Strawberry notch homolog 2 is a novel inflammatory response factor predominantly but not exclusively expressed by astrocytes in the central nervous system

GLIA

Volumn 63, Issue 10, 2015, Pages 1738-1752

  Grill, Magdalena ^a,b   Syme, Taylor E ^a   Noçon, Aline L ^a   Lu, Andy Z X ^a   Hancock, Dale ^a   Rose John, Stefan ^c   Campbell, Iain L ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY OF KIEL   (Germany)

Author keywords

Astrocyte; Cytokines; Glycoprotein 130; Inflammation; Strawberry notch homolog 2

Indexed keywords

ENDOTOXIN; GLYCOPROTEIN GP 130; INTERLEUKIN 11; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; REGULATOR PROTEIN; STRAWBERRY NOTCH HOMOLOG 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYCLOHEXIMIDE; CYTOKINE RECEPTOR; CYTOKINE RECEPTOR, GLM-R; PROTEIN SYNTHESIS INHIBITOR; REPRESSOR PROTEIN; SBNO2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN LEVEL; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; ENDOTOXEMIA; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; METABOLISM; NEWBORN; TIME FACTOR;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BRAIN; CELLS, CULTURED; CYCLOHEXIMIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; PROTEIN SYNTHESIS INHIBITORS; RECEPTORS, CYTOKINE; REPRESSOR PROTEINS; RNA, MESSENGER; TIME FACTORS; UP-REGULATION;

EID: 84938984903     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22841     Document Type: Article

References (56)

1. Baba K, Dekimoto H, Muraoka D, Agata K, Terashima T, Katsuyama Y. 2006. A mouse homologue of strawberry notch is transcriptionally regulated by Reelin signal. Biochem Biophys Res Commun 350:842-849.
2. Barnum SR, Jones JL, Mueller-Ladner U, Samimi A, Campbell IL. 1996. Chronic complement c3 gene expression in the CNS of transgenic mice with astrocyte-targeted Interleukin-6 expression. Glia 18:107-117.
3. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, Mucke L. 1993. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci USA 90:10061-10065.
4. Campbell IL, Hobbs MV, Kemper P, Oldstone MB. 1994. Cerebral expression of multiple cytokine genes in mice with lymphocytic choriomeningitis. J Immunol 152:716-723.
5. Campbell IL, Erta M, Lim SL, Frausto RF, May U, Rose-John S, Scheller J, Hidalgo J. 2014. Trans-signaling is a dominant mechanism for the pathogenic actions of interleukin-6 in the brain. J Neurosci 34:2503-2513.
6. Carter SL, Muller M, Manders PM, Campbell IL. 2007. Induction of the genes for cxcl9 and cxcl10 is dependent on IFN-gamma but shows differential cellular expression in experimental autoimmune encephalomyelitis and by astrocytes and microglia in vitro. Glia 55:1728-1739.
7. Chiang CS, Stalder A, Samimi A, Campbell IL. 1994. Reactive gliosis as a consequence of Interleukin-6 expression in the brain-Studies in transgenic mice. Dev Neurosci 16:212-221.
8. Chikuma T, Yoshimoto T, Ohba M, Sawada M, Kato T, Sakamoto T, Hiyama Y, Hojo H. 2009. Interleukin-6 induces prostaglandin E(2) synthesis in mouse astrocytes. J Mol Neurosci 39:175-184.
9. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
10. Coyle-Thompson CA, Banerjee U. 1993. The strawberry notch gene functions with Notch in common developmental pathways. Development 119:377-395.
11. Croker BA, Kiu H, Nicholson SE. 2008. SOCS regulation of the JAK/STAT signalling pathway. Semin Cell Dev Biol 19:414-422.
12. Croker BA, Krebs DL, Zhang JG, Wormald S, Willson TA, Stanley EG, Robb L, Greenhalgh CJ, Forster I, Clausen BE, Nicola NA, Metcalf D, Hilton DJ, Roberts AW, Alexander WS. 2003. Socs3 negatively regulates IL-6 signaling in vivo. Nat Immunol 4:540-545.
13. Damiani CL, O'Callaghan JP. 2007. Recapitulation of cell signaling events associated with astrogliosis using the brain slice preparation. J Neurochem 100:720-726.
14. El Kasmi KC, Smith AM, Williams L, Neale G, Panopoulos AD, Watowich SS, Hacker H, Foxwell BM, Murray PJ. 2007. Cutting edge: A transcriptional repressor and corepressor induced by the STAT3-regulated anti-inflammatory signaling pathway. J Immunol 179:7215-7219.
15. Ernst M, Jenkins BJ. 2004. Acquiring signalling specificity from the cytokine receptor gp130. Trends Genet 20:23-32.
16. Erta M, Quintana A, Hidalgo J. 2012. Interleukin-6, a major cytokine in the central nervous system. Int J Biol Sci 8:1254-1266.
17. Fischer M, Goldschmitt J, Peschel C, Brakenhoff JP, Kallen KJ, Wollmer A, Grotzinger J, Rose-John S. 1997. A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat Biotechnol 15:142-145.
18. Frei K, Fredrikson S, Fontana A, Link H. 1991. Interleukin-6 is elevated in plasma in multiple-sclerosis. J Neuroimmunol 31:147-153.
19. Hashimoto-Torii K, Torii M, Sarkisian MR, Bartley CM, Shen J, Radtke F, Gridley T, Sestan N, Rakic P. 2008. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60:273-284.
20. Herrmann JE, Imura T, Song B, Qi J, Ao Y, Nguyen TK, Korsak RA, Takeda K, Akira S, Sofroniew MV. 2008. Stat3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28:7231-7243.
21. Hutchins AP, Poulain S, Miranda-Saavedra D. 2012. Genome-wide analysis of stat3 binding in vivo predicts effectors of the anti-inflammatory response in macrophages. Blood 119:e110-e119.
22. Ip JP, Nocon AL, Hofer MJ, Lim SL, Muller M, Campbell IL. 2011. Lipocalin 2 in the central nervous system host response to systemic lipopolysaccharide administration. J Neuroinflamm 8:124.
23. Jones SA, Richards PJ, Scheller J, Rose-John S. 2005. IL-6 transsignaling: The in vivo consequences. J Interferon Cytokine Res 25:241-253.
24. Lang R, Pauleau AL, Parganas E, Takahashi Y, Mages J, Ihle JN, Rutschman R, Murray PJ. 2003. Socs3 regulates the plasticity of gp130 signaling. Nat Immunol 4:546-550.
25. Lust JA, Donovan KA, Kline MP, Greipp PR, Kyle RA, Maihle NJ. 1992. Isolation of an mRNA encoding a soluble form of the human interleukin-6 receptor. Cytokine 4:96-100.
26. Maier J, Kincaid C, Pagenstecher A, Campbell IL. 2002. Regulation of signal transducer and activator of transcription and suppressor of cytokine-signaling gene expression in the brain of mice with astrocyte-targeted production of interleukin-12 or experimental autoimmune encephalomyelitis. Am J Pathol 160:271-288.
27. Majumdar A, Nagaraj R, Banerjee U. 1997. Strawberry notch encodes a conserved nuclear protein that functions downstream of Notch and regulates gene expression along the developing wing margin of drosophila. Gene Dev 11:1341-1353.
28. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC Gonzales NR, et al. 2011. CDD: A conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225-D229.
29. Maruyama K, Uematsu S, Kondo T, Takeuchi O, Martino MM, Kawasaki T, Akira S. 2013. Strawberry notch homologue 2 regulates osteoclast fusion by enhancing the expression of DC-STAMP. J Exp Med 210:1947-1960.
30. März P, Cheng JG, Gadient RA, Patterson PH, Stoyan T, Otten O, Rose-John S. 1998. Sympathetic neurons can produce and respond to interleukin 6. Proc Natl Acad Sci USA 95:3251-3256.
31. März P, Heese K, Dimitriades-Schmutz B, Rose-John S, Otten O. 1999. Role of Interleukin-6 and soluble IL-6 receptor in region-specific induction of astrocytic differentiation and neurotrophin expression. Glia 26:191-200.
32. Mathieu ME, Saucourt C, Mournetas V, Gauthereau X, Theze N, Praloran V, Thiebaud P, Boeuf H. 2012. LIF-dependent signaling: New pieces in the lego. Stem Cell Rev 8:1-15.
33. Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T. 1994. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett 180:147-150.
34. Mullberg J, Dittrich E, Graeve L, Gerhartz C, Yasukawa K, Taga T, Kishimoto T, Heinrich PC, Rose-John S. 1993. Differential shedding of the two subunits of the interleukin-6 receptor. FEBS Lett 332:174-178.
35. Odemis V, Moepps B, Gierschik P, Engele J. 2002. Interleukin-6 and cAMP induce stromal cell-derived factor-1 chemotaxis in astroglia by up-regulating cxcr4 cell surface expression. Implications for brain inflammation. J Biol Chem 277:39801-39808.
36. Quintana A, Molinero A, Borup R, Nielsen FC, Campbell IL, Penkowa M, Hidalgo J. 2008. Effect of astrocyte-targeted production of IL-6 on traumatic brain injury and its impact on the cortical transcriptome. Dev Neurobiol 68:195-208.
37. Richards CD. 2013. The enigmatic cytokine oncostatin M and roles in disease. ISRN Inflamm 2013:512103.
38. Rose-John S. 2012. IL-6 trans-signaling via the soluble IL-6 receptor: Importance for the pro-inflammatory activities of IL-6. Int J Biol Sci 8:1237-1247.
39. Rose-John S, Heinrich PC. 1994. Soluble receptors for cytokines and growth factors: Generation and biological function. Biochem J 300:281-290.
40. Rose-John S, Scheller J, Elson G, Jones SA. 2006. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: Role in inflammation and cancer. J Leukoc Biol 80:227-236.
41. Sanz E, Hofer MJ, Unzeta M, Campbell IL. 2008. Minimal role for stat1 in interleukin-6 signaling and actions in the murine brain. Glia 56:190-199.
42. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. 2011. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 1813:878-888.
43. Sharova LV, Sharov AA, Nedorezov T, Piao Y, Shaik N, Ko MSH. 2009. Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res 16:45-58.
44. Simms CL, Baillie DL. 2010. A strawberry notch homolog, let-765/nsh-1, positively regulates lin-3/egf expression to promote RAS-dependent vulval induction in C. elegans. Dev Biol 341:472-485.
45. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
46. Spooren A, Kolmus K, Laureys G, Clinckers R, De Keyser J, Haegeman G, Gerlo S. 2011. Interleukin-6, a mental cytokine. Brain Res Rev 67:157-183.
47. Sriram K, Benkovic SA, Hebert MA, Miller DB, O'Callaghan JP. 2004. Induction of gp130-related cytokines and activation of jak2/stat3 pathway in astrocytes precedes up-regulation of glial fibrillary acidic protein in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine model of neurodegeneration: Key signaling pathway for astrogliosis in vivo? J Biol Chem 279:19936-19947.
48. Stalder AK, Pagenstecher A, Kincaid CL, Campbell IL. 1999. Analysis of gene expression by multiprobe RNase protection assay. In: Harry J, Tilson HA, editors. Methods in molecular medicine. Totowa, NJ: Humana Press. pp 53-66.
49. Stalder AK, Pagenstecher A, Yu NC, Kincaid C, Chiang CS, Hobbs MV, Bloom FE, Campbell IL. 1997. Lipopolysaccharide-induced IL-12 expression in the central nervous system and cultured astrocytes and microglia. J Immunol 159:1344-1351.
50. Takano A, Zochi R, Hibi M, Terashima T, Katsuyama Y. 2010. Expression of strawberry Notch family genes during zebrafish embryogenesis. Dev Dyn 239:1789-1796.
51. Takano A, Zochi R, Hibi M, Terashima T, Katsuyama Y. 2011. Function of strawberry notch family genes in the zebrafish brain development. Kobe J Med Sci 56:E220-E230.
52. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511-515.
53. Tsuda L, Nagaraj R, Zipursky SL, Banerjee U. 2002. An EGFR/ebi/sno pathway promotes delta expression by inactivating su(H)/SMRTER repression during inductive Notch signaling. Cell 110:625-637.
54. Van Wagoner NJ, Oh JW, Repovic P, Benveniste EN. 1999. Interleukin-6 (IL-6) production by astrocytes: Autocrine regulation by IL-6 and the soluble IL-6 receptor. J Neurosci 19:5236-5244.
55. Wang J, Schreiber RD, Campbell IL. 2002. Stat1 deficiency unexpectedly and markedly exacerbates the pathophysiological actions of IFN-alpha in the central nervous system. Proc Natl Acad Sci USA 99:16209-16214.
56. Wood JA, Wood PL, Ryan R, Graff-Radford NR, Pilapil C, Robitaille Y, Quirion R. 1993. Cytokine indices in Alzheimer's temporal cortex: No changes in mature IL-1/3 or IL-1RA but increases in the associated acute phase proteins IL-6, a2-macroglobulin and C-reactive protein. Brain Res 629:245-252.